Journal of Marine Systems 149 (2015) 5059

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Journal of Marine Systems

journal homepage: www.elsevier.com/locate/jmarsys

Estimating oceanic primary productivity from ocean color remote

sensing: A strategic assessment
Zhongping Lee a,, John Marra b, Mary Jane Perry c, Mati Kahru d
a
School for the Environment, University of Massachusetts Boston, Boston, MA 02125, USA
b
Aquatic Research and Environmental Assessment Center, Brooklyn College of the City University of New York, Brooklyn, NY 11210, USA
c
School of Marine Science, University of Maine, Darling Marine Center, University of Maine Walpole, ME 04573, USA
d
Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, USA

a r t i c l e i n f o a b s t r a c t

Article history: It has long been realized that approaches using satellite ocean-color remote sensing are the only feasible means
Received 30 September 2013 to quantify primary productivity (PP) adequately for the global ocean. Through decades of dedicated efforts and
Received in revised form 27 November 2014 with the help of various satellite ocean-color missions, great progresses have been achieved in obtaining global
Accepted 30 November 2014
PP as well as its spatial and temporal variations. However, there still exist wide differences between satellite
Available online 19 December 2014
estimations and in situ measurements, as well as large discrepancies among results from different models. The
Keywords:
reasons for these large differences are many, which include uncertainties in measurements, errors in satellite-
Primary productivity derived products, and limitations in the modeling approaches. Unlike previous round-robin reports on PP
Ocean optics modeling where the performance of specic models was evaluated and compared, here we try to provide a
Ocean color remote sensing candid overview of three primary modeling strategies and the nature of present satellite ocean-color products.
We further highlight aspects where efforts should be focused in the coming years, with the overarching goal of
reducing the gaps between satellite modeling and in situ measurements.
2014 Elsevier B.V. All rights reserved.

1. Introduction
Photosynthesis is a process that occurs on the illuminated Earth. In a
complex light-dependent process, photosynthesis transfers absorbed
photon energy to organic compounds (Falkowski and Raven, 2007).
Since this process ultimately leads to the conversion of inorganic carbon
to organic carbon, photosynthesis not only plays an important role in
the global carbon cycle, but also provides the food to support all
the heterotrophs. In the ocean, phytoplankton are the primary
photosynthesizers, supporting the ocean's food web. As realized
~ 50 years ago (Goldman, 1965), because of the vast expanse of the
oceans, detailed information about the temporal and spatial variation
of oceanic photosynthesis is essential for studying and understanding
airsea CO2 exchange, carbon xation, and vertical export the so
called biological pump (Antoine et al., 1996; Behrenfeld et al., 2002;
Bosc et al., 2004; Dunne et al., 2005; Falkowski et al., 2003; Nevison
et al., 2012; Platt and Sathyendranath, 1988; Sathyendranath et al.,
1995).
The production of organic carbon during photosynthesis is dened
as primary productivity (PP, or net primary productivity, NPP; Cullen,
2001; Marra, 2002; Platt and Sathyendranath, 1993). In the ocean, PP
provides a measure of inorganic carbon xed by phytoplankton per
Corresponding author.
E-mail address: zhongping.lee@umb.edu (Z. Lee).
unit of water volume per unit of time. Integration of this rate over
desired basins and for a given period of time (e.g., a year) provides a
measure of carbon transformation for that area for that time period. It
has been and remains an elusive goal for researchers in biological
oceanography to obtain accurate and consistent estimates of PP for
the global oceans. Beside limitations in measurement technology
(Cullen, 2001; Marra, 2002; Platt and Sathyendranath, 1993), the
major limitation is the extreme under sampling of the oceans (Perry,
1986), where the spatial and temporal variations in water properties
(including optical, chemical, and biological, etc.) cannot be easily
scaled-up from a few measurements made at limited spacetime grids.
To overcome such spatialtemporal limitations, it has long been rec-
ognized that the repetitive measurement by satellite sensors provides
the only possible and feasible means for the estimation of PP on basin
and global scales (Eppley et al., 1985; Falkowski, 1998; Perry, 1986;
Platt, 1986), i.e., to obtain estimates at large scales by linking discrete
in situ measurements with the synoptic and repetitive satellite observa-
tions. The linkage for this scaling-up, as discussed in detail in later sec-
tions, is centered on information on phytoplankton (either a biological
property such as chlorophyll concentration or an optical property such
as phytoplankton absorption coefcient). This is based on the fact that
phytoplankton not only plays a key role in photosynthesis, but also
alters the appearance of ocean (water) color. Therefore, when a rela-
tionship between PP and phytoplankton is developed, the estimation
of basin-scale PP becomes possible when the information of

http://dx.doi.org/10.1016/j.jmarsys.2014.11.015
0924-7963/ 2014 Elsevier B.V. All rights reserved.
 Z. Lee et al. / Journal of Marine Systems 149 (2015) 5059
phytoplankton can be derived from the measurement of ocean color by
a satellite sensor. Because of this necessity, the estimation of the global
phytoplankton (and then oceanic PP) is a central goal of all ocean-color
satellite missions (IOCCG, 1998; McClain, 2009), which include the Sea-
Viewing Wide Field-of-View Sensor (SeaWiFS) and the MODerate-
resolution Imaging Spectroradiometer (MODIS) supported by NASA,
and the Medium Resolution Imaging Spectrometer (MERIS) supported
by ESA. In addition, new and advanced ocean color satellites are on
the horizon, including the Pre-Aerosol Cloud and Ecosystems (PACE,
NASA) mission and the Ocean and Land Colour Instrument (OLCI,
ESA). At the same time, in order to properly scale-up the limited
eld measurements with satellite data, various models have been
developed (e.g., Antoine and Morel, 1996; Arrigo et al., 2008; Balch
et al., 1989b; Behrenfeld, 1998; Dierssen et al., 2000; Ishizaka,
1998; Kahru et al., 2009; Longhurst et al., 1995; Ondrusek et al.,
2001; Sathyendranath and Platt, 1995; Sathyendranath et al., 1989;
Sathyendranath et al., 1991) and estimates of global oceanic PP
have been achieved (Antoine et al., 1996; Behrenfeld et al., 2002;
Longhurst et al., 1995; Platt and Sathyendranath, 1988).
After decades of practice, however, the estimates based on satel-
lite remote sensing are far from satisfactory. For instance, results
from the Joint Global Ocean Flux Study (JGOFS) (Ducklow, 2003)
have found that, in four of eight oceanic provinces (Longhurst
et al., 1995) where data are available for PPbasin-year (basin-scale, annual,
depth-integrated primary production) from both in situ measurements
and from the measurements of the Coastal Zone Color Scanner (CZCS),
the satellite estimates were a factor of two or three smaller than the
measured values. In only two out of the eight provinces were the
CZCS PPbasin-year within 20% of the measured values. If the comparison
is made on local-daily instead of basin-year scales regarding the spatial
and time ranges, the disagreement could be much larger between mea-
sured and ocean color-derived PPeu (daily depth-integrated primary
production) as shown in some studies (e.g., Balch et al., 1989a;
Behrenfeld and Falkowski, 1997b; Quay et al., 2012), although better
results were presented in Platt and Sathyendranath (1988) and
Kyewalyanga et al. (1997).
The discrepancies between modeled and measured PP, and among
modeled PP, were also highlighted in a series of round-robin experi-
ments (Campbell et al., 2002; Carr et al., 2006; Friedrichs et al., 2009).
Even with measured chlorophyll concentration as an input, Campbell
et al. (2002) found that PP estimates from the best-performing algo-
rithms were generally within a factor of 2 of measured PP; while Carr
et al. (2006) found that global average PP varied by a factor of 2 between
models when input parameters (chlorophyll concentration and solar ra-
diation) were derived from SeaWiFS. For a dataset consisting of ~1000
in situ measurements in the tropical Pacic, Friedrichs et al. (2009)
found that all models underestimated the observed variance of PP,
and no models successfully captured a broad-scale shift from low
biomass-normalized productivity in the 1980s to a higher biomass-
normalized productivity in the 1990s.
Such inconsistent results undermine the condence of using prima-
ry production estimated from satellite ocean color to study the biolog-
ical pump in the oceans, and suggest that there is difcult work ahead
in designing the strategy and system for estimating primary production
based on remotely sensed data. Here we try to provide a candid over-
view of the strategies in estimating PP from ocean color remote sensing,
discuss the status of standard satellite ocean-color products, and high-
light areas where efforts should be focused on for improving the estima-
tion of PP from satellite ocean color remote sensing.
2. Principles of ocean color remote sensing
It has been known for centuries that the change of water (ocean)
color reects change of constituents in the water column. To be able
to quantitatively, and mechanistically, estimate the constituent concen-
trations, models have been developed to link ocean color with desired
51
constituents. In ocean color remote sensing, ocean color is commonly
described with the spectrum of remote-sensing reectance (Rrs(),
sr 1), which is dened as the ratio of water-leaving radiance to
downwelling irradiance just above the surface. Water-leaving radi-
ance represents photons originating from absorption and scattering
processes below the surface and emitting into space, which excludes
photons going to space due to sea-surface reectance, a process having
no information of in-water constituents.
Based on the radiative transfer theory, Rrs can be expressed as
(Gordon et al., 1988; Sathyendranath and Platt, 1997; Zaneveld, 1995)


bb bb
Rrs 0:53 g 0 g 1 : 1
a bb a bb
Here a and bb are the total absorption and backscattering coefcients,
respectively, and wavelength dependence is omitted for brevity. g0
and g1 are model coefcients, which are spectrally independent,
although slightly varying with sun-sensor angular geometry (Albert
and Mobley, 2003; Lee et al., 2011a; Morel and Gentili, 1993).
a and bb are bulk inherent optical properties (IOPs) (Preisendorfer
and Mobley, 1984), which are sums of the contributions of various con-
stituents (Stramski et al., 2001), with the primary components as water
molecules, suspended particulates and dissolved materials (also termed
as gelbstoff, etc.). Practically, the bulk IOPs are generally described as
a aw aph adg ;
2
bb bbw bbp ;
with subscripts w, ph, dg, p representing water, algae pigments, the
combination of detritus and gelbstoff, and particles, respectively. Values
of aw and bbw have been measured or derived from laboratory or eld
measurements (Morel, 1974; Pope and Fry, 1997; Smith and Baker,
1981), and are considered global constants (vary slightly with temper-
ature and salinity) (Pegau et al., 1997; Sullivan et al., 2006). aph, adg
and bbp, on the other hand, vary spatially and temporally, and are
considered as volatile properties.
For studies in ocean biology and biogeochemistry, traditionally the
focus of ocean color remote sensing is on the concentration of chloro-
phyll, thus the component IOPs are commonly expressed as
 
a aw aph  Chl GChl  aph  Chl;
 3
bb bbw bbp  Chl:
Here aph and bph are the chlorophyll-specic (or concentration of chlo-
rophyll normalized) absorption and chlorophyll-specic backscattering
coefcients (m2/mg), respectively, with Chl the concentration of
chlorophyll (mg/m3). GChl is the ratio (at a specic wavelength, such
as 440 nm) of adg to aph.
Therefore, if values of aph , bbp and GChl are known, or if they co-vary
with Chl, Eq. (1) is a function of one variable: Chl, which can then be
solved from known Rrs. Because particle backscattering coefcient
(bbp) could not be accurately modeled with Chl alone (see Stramski
et al., 2001), bbp encompasses a wide range of variations for a given
Chl (Babin et al., 2003; Loisel and Morel, 1998). To minimize the impact
of this variation on the retrieval of Chl from Rrs, usually the band ratio of
Rrs (either blue to green, or red to green; Le et al., 2013) is used as input,
with a general form as (Gordon and Morel, 1983; O'Reilly et al., 1998)
   
Chl f 1 Rrs i =Rrs j : 4
Here f1 stands for function number 1. Following Eqs. (23), in essence
the above ratio algorithm includes (assuming the impact of parameter
bbp is minimized through the Rrs ratio), implicitly, variables other
than the ratio of Rrs (Carder et al., 1999; Gordon et al., 1988;
Sathyendranath and Platt, 1989; Sathyendranath et al., 1994)
  
Chl f 1 aph ; GChl ; Rrs i =Rrs j : 5
52 Z. Lee et al. / Journal of Marine Systems 149 (2015) 5059
This simplied, but general, conceptual relationship clearly indicates
the fundamental dependence of Chl retrieval on the values of aph and
GChl.
On the other hand, if the focus on the retrieval is IOPs, the ratio of Rrs
is
 
Rrs i =Rrs j
0      1
bbw i bbp i aw j aph j adg j
f 2@     A;
bbw j bbp j aw i aph i adg i
where the concentration-normalized parameters are not involved, thus
lower uncertainty in retrieving IOPs is expected (Lee et al., 1998), at
least in theory.
3. Basics of primary productivity modeling
As dened earlier, primary productivity quanties xed carbon from
photosynthesis, which represents a transfer of absorbed photon energy
to organic carbon (note: we recognize that not all reductants produced
from absorbed photon energy are used in reduction of CO2, but rather in
the reduction of nitrate and other compounds). Because chlorophyll-a
pigment is critical for the photosynthesis process, a generalized
conceptual model for this quantication has commonly been written
as (Bannister, 1974; Behrenfeld and Falkowski, 1997a; Eppley et al.,
1985; Platt and Sathyendranath, 1988; Ryther, 1956)

PP  aph  Chl  E;
with E for available photon energy (representing photosynthetic avail-
able radiation, PAR, 400700 nm, quanta/m2). The product of aph , Chl,
and E is the absorbed photon energy by phytoplankton. (the photo-
synthetic quantum yield) represents the efciency factor for the conver-
sion of the absorbed photon energy to organic carbon (essentially, the
energy stored in organic carbon; Morel, 1978). The product of and
aph (represented by in the following equation) is commonly termed
as biomass-normalized (or chlorophyll-normalized) photosynthesis
rate, and Eq. (7) is also commonly written as (Behrenfeld and
Falkowski, 1997a):
PP  Chl  E:
Because light penetrates deep below the sea surface and changes
spectrally with depth, impact from both depth and wavelength must
also be included. A generalized wavelength-resolved model for the
quantication of primary production can be expressed as (Behrenfeld
and Falkowski, 1997a; Sathyendranath and Platt, 1988)
PPz z  Chlz  E; zd; 9 Gordon and Morel, 1983; Gordon et al., 1983). Presently, as discussed
with PP(z) representing the primary production at depth z, and the inte-
gration of PP(z) over depth provides a measure of the photosynthesis of
the whole water column. Based on the radiative transfer equation, the
propagation of light in the water column can be expressed as
E; z E; 0e
K z
; 10
with E(,0) for spectral light energy just below the surface and K() the
spectral diffuse attenuation coefcient (m1) for E(). Because this sys-
tem has Chl as the core input (K() can be modeled from Chl for Case-1
waters (Morel, 1988; Morel and Maritorena, 2001)), this scheme is
termed as the Chl-based approach (Behrenfeld et al., 2005).
The implication of Eqs. (9) and (10) is quite clear; the desired quan-
tities for modeling PP(z) are three variables: E, Chl, and . Studies have
shown that both E and Chl can be either measured easily in situ or esti-
mated from remotely sensed ocean color. If variable can be
characterized and parameterized, products of E and Chl thus provide
the linkage to scale-up discrete in situ PP measurements to basin-scale
PP estimations. To meet this demand, models for the estimation of
E(0) have been developed in the past decades (Frouin et al., 1989;
Frouin et al., 2003; Gregg and Carder, 1990; Journe and Bertrand,
2010; Van Laake and Sanchez-Azofeifa, 2005). There have been enor-
mous efforts to develop algorithms for the retrieval of Chl from ocean
color measurements (e.g., Bukata et al., 1981; Carder et al., 1999;
6 Dall'Olmo and Gitelson, 2005; Devred et al., 2005; Doerffer and Fisher,
1994; Gordon and Morel, 1983; Hu et al., 2012b; Le et al., 2013;
Mitchell and Holm-Hansen, 1990; Morel et al., 2006; O'Reilly et al.,
1998; Sathyendranath et al., 2005). Additionally, eld studies have fo-
cused on characterization and parameterization of the variable (e.g.,
Cullen, 1990; Cullen et al., 1992; Marra and Barber, 2005; Platt et al.,
1980). Many different forms and models for the Chl-normalized photo-
synthesis rate have been reported (Falkowski and Raven, 2007;
Sakshaug et al., 1997), but Platt (1986) and Sathyendranath and Platt
(1995) have found that most of those equations yield similar results
for water-column integrals of primary production.
4. Discussion of applying current ocean-color products with the
Chl-based approach
Based on Eqs. (9) and (10), the estimation of basin-scale primary
production requires inputs of , E(0), Chl and K. And, because of this de-
mand, there have been thousands of concurrent measurements of PP, E,
and Chl in the past decades (Behrenfeld and Falkowski, 1997b; Platt
7 et al., 1991). Variation of depends on phytoplankton physiology, its
value cannot be directly provided from ocean color remote sensing,
but has to be estimated and modeled based on laboratory and/or eld
measurements. E(0) can be determined with information on sun posi-
tion and atmospheric properties. Chl and K, however, are bio-optical
properties that are derived from the measurement of ocean color, em-
pirically or semi-analytically. These features frame the basic logic why
E(0), Chl and K (but limited to Kd(490) at present) are standard products
of all satellite ocean color missions (e.g., http://oceancolor.gsfc.nasa.gov/
cgi/l3?per=DAY). However, as discussed in details below, these stan-
dard ocean-color products are not straightforwardly applicable for a
PP model like Eq. (9) for such estimations.
8 4.1. Standard product of Chl
Chl is a key input for PP modeling (see Eqs. (710)), hence an accu-
rate Chl retrieval from satellite ocean color remote sensing is critical for
the estimation of global PP (Behrenfeld and Falkowski, 1997a, b). Due to
its importance, tremendous efforts have been focused on the develop-
ment of algorithms for the derivation of Chl from ocean color data dating
back to the CZCS era (Bukata et al., 1981; Doerffer and Fisher, 1994;
earlier, the standard satellite Chl product is still derived from the band
ratio of Rrs, with a general form as Eq. (4). However, as depicted by
Eq. (5), to get Chl from the Rrs band-ratio, not only the GChl value has
to be specied (or has to co-vary with Chl), the value of aph need also
be known (or co-vary with Chl). In the empirical algorithm for the
standard Chl product (O'Reilly et al., 1998), the values (or variations)
of GChl and a ph are not specied, but embedded implicitly in the
algorithm coefcients. In other words, such values or variations are
implicitly treated as universally stable constants or dependances. On
the other hand, numerous eld studies (Babin et al., 1993; Bricaud
and Morel, 1986; Bricaud et al., 1981; Bricaud et al., 1995; Carder
et al., 1986; Carder et al., 1989; Carder et al., 1991; Carder et al., 1999;
Carder et al., 2004; Cleveland, 1995; Del Castillo et al., 2000; Kirk,
1994; Lutz et al., 1996; Mitchell and Kiefer, 1988; Morel and Bricaud,
1981; Sathyendranath et al., 1987; Sosik and Mitchell, 1995; Stuart
et al., 1998) have pointed out that both GChl and aph are not constants
even for oceanic waters, and there are no xed values for either GChl
 Z. Lee et al. / Journal of Marine Systems 149 (2015) 5059
or aph for a given Chl. As a result, the empirical algorithms developed
from such globally and seasonally inclusive datasets tend to produce re-
gional biases, which further obscure the spatial and temporal character-
istics of Chl in the global oceans (Brown et al., 2008; Szeto et al., 2011).
This might not be too surprising because the spectral variation of bb
is mild compared to the spectral variation of a, so a change of the Rrs
ratio indicates mostly a change of the absorption coefcient. Therefore,
the so-called Chl product is indeed an index of this bulk absorption
coefcient (comparing Eq. (4) with Eq. (6)) and can be written as
Chl f 2 a: 11
This fundamental relationship indicates that the standard Chl product
does not match the desired chlorophyll-a required in a Chl-based PP
model (e.g., Eq. (8)), where the model was developed based on real
chlorophyll-a a biological property, not the total absorption coef-
cient an optical property. This mismatch helps explain a conclusion
in Saba et al (2011) that ocean color models did not accurately estimate
the magnitude of the trends of NPP over multidecadal time periods, and
were even more challenged over shorter time periods, especially when
the models used satellite-derived Chl-a.
4.2. Uncertainties of
Prior studies (Balch et al., 1992; Behrenfeld and Falkowski, 1997b)
have pointed out that even with in situ measured Chl, PP can only be
quantied with an accuracy of at best 5060%. This is because whenever
PP is modeled with Chl as a scaling parameter (see Eq. (8)), it automat-
ically requires the specication of or a similar Chl-normalized photo-
synthetic parameter (such as biomass-normalized growth rate). More
specically, the biomass- (or chlorophyll-) normalized photosynthesis
parameter is (Behrenfeld and Falkowski, 1997a; Cullen, 1990)

 aph : 12
The quantum yield of photosynthesis () and aph are, in principle, two
independent properties, and both vary spatially and temporally. This
nature helps explain why a PP model may not perform well even with
measured Chl as input. As discussed earlier, due to variations in pigment
composition and the package effect (Bidigare et al., 1990; Bricaud
et al., 1988; Hoepffner and Sathyendranath, 1991), aph can vary over a
factor of 4 or more for the same Chl value (Bricaud et al., 1995). This
indicates that the biomass-normalized photosynthesis rate will
fundamentally vary signicantly for a given Chl (Platt et al., 2008). Con-
sequently, without knowing the aph value associated with the develop-
ment of the PP model, a mismatch in the aph will result in different
(assuming values are the same), and then different PP even if Chl
and E values are the same. This natural variability, at least partially,
explains a conclusion of Behrenfeld and Falkowski (1997b) that signif-
icant improvements in estimating oceanic primary production will not
be forthcoming without considerable advance in our ability to predict
B B
temporal and spatial variability in Popt . Note that Popt is similar to as
a biomass-normalized parameter (Falkowski, 1998). The same conclu-
sions can also be found from other modeling studies (Morel et al.,
1996; Sosik, 1996). It is quite a challenge to reach this goal from remote
sensing though, because there is no reliable method as yet to accurately
B
estimate the spatial and temporal variation of Popt from satellite
measurements.
4.3. Light-related products
Photosynthesis needs light, and it might be envisioned that the
combination of E(0) and Kd(490) products can somehow provide the
necessary input of solar radiation at depth. However, a few caveats
prevent a direct application of these standard ocean color products for
the estimation of E(z). These include the following:
53
1) The algorithm used for the generation of Kd(490) was developed in a
similar fashion as for the retrieval of Chl, i.e., by pulling together glob-
al datasets to produce the best empirical relationship between the
desired product and Rrs band-ratio. Although the Rrs-ratio does re-
ect optical properties (see Eq. (6)), the practice overlooked, or
ignored, a fundamental feature that Kd is an apparent optical proper-
ty (AOP) (Preisendorfer, 1976). Unlike Chl, Kd can differ by more
than 40% between the sun at zenith and the sun just above the hori-
zon (Gordon, 1989; Kirk, 1984; Sathyendranath and Platt, 1988).
Consequently, the empirically-derived Kd(490) is best for sun
positions matching the mode of the dataset used for the algorithm
development (Lee et al., 2013), but will result in large errors for
other sun angles, even assuming that the algorithm is perfect.
2) Kd(490) is for light attenuation at one wavelength only, which
cannot be applied for the attenuation of photosynthetic available ra-
diation (PAR), a broad-band (usually 400700 nm) radiometric
quantity. A separate attenuation product, called Kd(PAR), has also
been developed empirically (Morel and Maritorena, 2001; Morel
et al., 2007). This Kd(PAR), however, in addition to having the
same sun-elevation issue as that of Kd(490), is only good for the es-
timation of PAR at depth where PAR(z) is 1% of PAR(0) (Morel et al.,
2007). This is because Kd(PAR) varies signicantly (a factor of 3 or
more) with depth even for vertically well-mixed waters (Lee,
2009; Morel, 1988; Zaneveld et al., 1993). Thus the Kd(PAR) value
for one depth interval cannot be used for the estimation of broad-
band radiation at other depths.
3) E(0) is either an instantaneous product or a daily product (Frouin
et al., 1989; Frouin et al., 2012). Kd(490) and Kd(PAR), on the other
hand, as discussed above, are valid for their own specic sun eleva-
tions, and thus cannot be directly applied with the E(0) product for
the estimation of daily E(z) unless there is a match in solar elevation.
In summary, the present E(0) and Kd products of satellite ocean color
missions are not directly applicable for an accurate estimation of E at
depth. For easy and straightforward estimation of solar radiation in
the upper water column, it is necessary to generate a new set of optical
products from ocean color remote sensing.
5. Carbon-based algorithm to estimate primary productivity
Another scheme, the carbon-based approach (Behrenfeld et al.,
2005) has also been developed, where PP can be estimated as
PP eu C   Z eu  f 3 E; 13
with PPeu the water-column integrated productivity, C for phytoplank-
ton carbon, the growth rate, Zeu the euphotic-zone depth (practically
dened as the depth where the solar radiation is 1% of its surface
value), and f3(E) a parameter related to light-adjusted physiology
(Behrenfeld et al., 2005). In this system, C is converted from bbp, and
is described as a function of the ratio of Chl to C (Behrenfeld et al.,
2005). Such an approach removes any dependence on some empirical
value for assimilation efciency, and allows one to distinguish between
growth rate, light, and biomass driven changes in chlorophyll
(M. Behrenfeld, personal communication). The derived PPeu, however,
is mostly proportional to Chl because the C component is more or less
mathematically canceled out (less so in the later updated version;
Westberry et al., 2008).
The model of Arrigo et al. (1998, 2008) could also be put in this
category as the estimated PP(z) is proportional to the product of Chl
and C/Chl, although the net biomass-specic growth rate is modulated
with temperature and light. The C/Chl ratio, however, is set as a constant
(75 or 88.5 g:g), then the PP(z) estimated from this model is in general
also proportional to Chl. Therefore, when the standard Chl product from
ocean color remote sensing is used, the derived primary productivity
represents mainly a conversion of the total absorption coefcient (see
54 Z. Lee et al. / Journal of Marine Systems 149 (2015) 5059
Eq. (11)), and large uncertainties will thus remain (Lee et al., 2011b)
because the variability associated with the spatialtemporal changes
of aph is not removed. This aph impact could be reduced if a regional-
and temporal-specic Chl algorithm is developed and implemented
(Arrigo and Sullivan, 1994; Arrigo et al., 1994).
Because of such a complex impact from aph on the estimation of PP
from ocean color remote sensing, large uncertainties in estimated PPeu
result. Siegel et al. (2001) found that Site-specic and previously
published global models of primary production both perform poorly
and account for less than 40% of the variance in PP, and the series of
round robin reports (Campbell et al., 2002; Carr et al., 2006; Friedrichs
et al., 2009) also found a large difference in spatial distributions of global
primary production from PP models that use Chl as a critical input
parameter.
There are also efforts to implement phytoplankton class- (or taxon-)
specic photosynthesis parameters (Alvain et al., 2006; Claustre et al.,
2005; Mouw and Yoder, 2005; Uitz et al., 2010), which may reduce
the impact of aph as different aph and values might be assigned to dif-
ferent class or taxon groups. But we are at an early stage to properly set
class- or taxon-specic values and to sense phytoplankton class
groups accurately from the measurement of ocean color.
6. Strategy centered on phytoplankton absorption
Because aph is a ratio of the phytoplankton absorption coefcient to
Chl, a mathematical manipulation of the parameters in Eq. (9) results in
a generalized model for primary productivity at depth as (Kiefer and
Mitchell, 1983)
Z
PP z z  aph z;  Ez; d: 14
In this model, the required phytoplankton-related input is aph instead of
Chl. That means, when is determined, the parameter needed for scale-
up in situ PP is aph (in addition to E) an optical property, instead of
Chl a biological property (Marra et al., 2007). This optical attribute
matches that of ocean-color remote-sensing, where the direct deriva-
tives will always be optical properties. In other words, the physiology
() and optical actions (aph) associated with photosynthesis are de-
scribed with two separate parameters in this scheme, whereas they
are tangled in both and Chl in the Chl-based approaches. More
specically, there will be no more need to specify the value of aph in
this aph-based approach when estimating PP from ocean color remote
sensing, thus avoiding one of the biggest uncertainty sources. To imple-
ment this strategy for the scale-up of primary production in basin scales,
it thus requires information on the following:
1) The light at the sea surface: E(0)
2) Absorption coefcient of phytoplankton pigments: aph
3) Light attenuation coefcient: K
4) Quantum yield: .
E(0) is independent of the PP models and is a standard product for all
ocean color missions. Although there are no standard products of aph
from satellite ocean-color sensors yet, algorithms (empirical or semi-
analytical) to derive aph from Rrs have been under development and
evaluation in the past decades (e.g., Carder et al., 1991; Carder et al.,
1999; Carder et al., 2004; Hoge and Lyon, 1996; IOCCG, 2006; Lee and
Carder, 2004; Lee et al., 1998; Lee et al., 2002; Roesler and Perry,
1995; Smyth et al., 2006). Further, semi-analytical models have been
developed for the estimation of spectral K from spectral IOPs (Lee
et al., 2005; Lee et al., 2013; Sathyendranath and Platt, 1988). Therefore,
the optical components associated with the quantication of photosyn-
thesis, at least the bulk IOPs, can be well retrieved from ocean color
measurements. Also, there has been quite a long history (e.g.,
Bannister and Weidemann, 1984; Bidigare et al., 1987; Carder et al.,
1995; Cleveland et al., 1989; Culver and Perry, 1999; Hiscock et al.,
2008; Kiefer and Mitchell, 1983; Kishino et al., 1986; Marra et al.,
1992; Marra et al., 2000; Morel, 1978; Smith et al., 1989; Sorensen
and Siegel, 2001; Wozniak et al., 2002) in the determination of the
quantum yield for photosynthesis (). Furthermore, techniques to
make routine measurements of optical properties (including aph) have
also advanced signicantly in the past decades (Allali et al., 1995;
Bricaud and Stramski, 1990; Kishino et al., 1985; Mitchell et al., 2002;
Roesler, 1998; Zaneveld et al., 1994), thus it is now feasible to use an op-
tical property (aph), instead of a biological property (Chl), as the linkage
parameter to scale-up discrete in situ PP measurements for global scale
estimates (Marra et al., 2007). Preliminary results with this scheme
(Hirawake et al., 2011; Lee et al., 1996; Lee et al., 2011b) do support
that modeling based on Eq. (14) provides promising potentials for
basin-scale PP estimation from satellite ocean color remote sensing.
7. Focus for future studies
We have discussed three strategies for the estimation of basin-scale
primary production from satellite ocean-color remote sensing. The
three strategies are separated by their two different foci: two on the
concentration of chlorophyll (Chl), and one on the absorption by phyto-
plankton (aph). In ocean-color remote sensing, aph, an optical property,
can be directly derived from Rrs; while Chl values can only be inferred
from aph or Rrs. Such general pictures indicate that, at least in theory,
estimation of PP centered on aph will involve less uncertainty. To imple-
ment such a strategy for the estimation of basin-scale PP, it requires
community efforts with objectives discussed in the following sections.
7.1. Improving measurement and retrieval of aph
Because the accuracy of modeling PP is strongly dependent on the
accuracy of remotely derived Chl or aph, in addition to improving satel-
lite sensor's sensitivity (Hu et al., 2001; Hu et al., 2012a), calibration
(Bailey et al., 2008; Eplee et al., 2001; Franz et al., 2007; Gordon,
1998) and atmospheric correction (Antoine and Morel, 1999; Gao
et al., 2000; Gordon, 1997; Gordon and Wang, 1994; Wang and Shi,
2007), all strategies require major efforts to improve algorithms for
the derivation of these properties from ocean-color data. Though Chl
and aph are two different kinds of properties (one biological and the
other optical), they both depend on accurate Rrs for their derivations,
no matter if the algorithm is semi-analytical or empirical. The analytical
retrieval of aph is associated with spectral modeling of bbp and adg ,
neither of which has a spectrally constant shape for the global waters.
In particular, usually aph is derived mechanistically from ocean color in-
formation at the blue-green bands, and it requires accurate description
of the detritusgelbstoff spectral dependence (Lee et al., 2010;
Maritorena and Siegel, 2005). Schemes to improve the modeling of
the spectral shapes of both bbp and adg are needed. An effective strategy
that divides the global ocean into dynamic-biogeochemical provinces
(Ducklow, 2003; IOCCG, 2009; Moore et al., 2001; Platt et al., 1991;
Sathyendranath et al., 1995) may improve the description of these
spectra and facilitate the derivation processes. To achieve this, it re-
quires adequate support from various agencies to carry out comprehen-
sive eld measurements in various regions of the global oceans.
For waters where the contribution of adg to the total absorption (at
440 nm) is much higher, say, a factor of 2 or more than that of aph, the
retrieval of aph using the optical information in the blue-green bands
runs into difculties (Lee et al., 2010). It is necessary to develop new
algorithms for the retrieval of aph for such waters. One scheme for the
retrieval of aph under such conditions is to use signals of chlorophyll-a
uorescence (e.g., Abbott and Letelier, 1999; Gower et al., 1999; Hoge
et al., 2003; Huot et al., 2005; Yentsch and Yentsch, 1979). This will re-
quire improved understanding of chlorophyll-a uorescence efciency
(Behrenfeld et al., 2009; Culver and Perry, 1997; Huot et al., 2005;
McKee et al., 2007).
 Z. Lee et al. / Journal of Marine Systems 149 (2015) 5059
In addition to algorithms to retrieve aph from ocean color data, aph
determined from eld measurements still has large uncertainties
(Allali et al., 1995; Bricaud and Stramski, 1990; Mitchell et al.,
2002; Mueller et al., 2003; Tassan and Ferrari, 1995), and there is
no universally accepted standard method for determining phytoplank-
ton pigment absorption.
7.2. Improving the estimation of diurnal radiation
It is necessary to note that frequently and variably, the Earth surface
is covered by clouds that greatly impact the photosynthesis of the Earth
system (Belanger et al., 2013; Graham et al., 2003). A Low Earth Orbit
(LEO) sensor normally has about one visit per day for an area of interest.
Therefore LEO observations will not be able to capture the diurnal pho-
tosynthesis of the upper water column. Such a sampling limitation will
not only affect the estimation of daily E(0) (Frouin et al., 2003), it will
also cause errors in the longer-time scale estimates of PP as photosyn-
thesis is not a linear function of E(0) (Behrenfeld and Falkowski,
1997a; Cullen, 1990; Kiefer and Mitchell, 1983; Sathyendranath and
Platt, 1995). In addition, cloud coverage modies the existence of UV
light at the surface and in the water column (Bartlett et al., 1998;
Mitchell and Lubin, 2003; Smyth, 2011), and UV light has a profound
impact on photosynthesis (e.g., Arrigo and Brown, 1996; Conde et al.,
2000; Cullen and Neale, 1994; Gao et al., 2012; Lorenzen, 1979;
Mitchell and Lubin, 2003; Smith and Cullen, 1995). It is thus necessary
to model the impact of the diurnal variation of UV light on the estima-
tion of PP. In addition, because light history always affects photo-
physiology and photosynthesis (Cullen et al., 1992; Falkowski and
Raven, 2007; Guasch and Sabater, 2002; Perry, 1986; Platt et al.,
1980), there is a clear demand to develop PP models that take into
account the diurnal variation of solar radiation and photosynthesis
(e.g., Arrigo et al., 1998; Arrigo et al., 2008), where measurements
from geostationary platforms will be useful signicantly (IOCCG,
2012; Perry, 1986).
7.3. Improving the determination of quantum yield ()
For the photosynthesis parameters, extensive studies (e.g., Balch and
Byrne, 1994; Behrenfeld and Falkowski, 1997b; Cullen et al., 1992;
Lohrenz et al., 1997, 1999; Platt, 1986; Platt et al., 1980; Sosik, 1996)
have been carried out on the variation of (or B and PBm, the
biomass-normalized initial rate and biomass-normalized maximum
photosynthesis), although no robust model yet to describe the variation
of these parameters with nutrient, temperature, and light histories. For
, there has been a long history of in situ measurements, but it is still far
from known how (in particular the maximum quantum yield, m)
varies for different ecosystems. Especially, there is no reliable model
yet to describe the spatial and temporal variations of for the global
oceans.
In addition, not all the phytoplankton absorbed photons participate
in photosynthesis (Falkowski and Raven, 2007; Perry et al., 1981), so a
more appropriate expression of Eq. (14) should be written as
PP  apsp  E; 15
with apsp the absorption coefcient of photosynthetic pigments (note
that wavelength and depth are omitted for brevity). It is thus necessary
to develop methodologies/algorithms to separate this absorption prop-
erty from aph (e.g., Bidigare et al., 1990; Hoepffner and Sathyendranath,
1993). On the other hand, the measurement of aph could be much easier
and straightforward than the measurement of apsp in the eld. In such a
case, it is important to clearly specify the absorption coefcient (aph or
apsp) used for the derivation of in the eld. In short, we need to
know how varies spatially and temporally, and to know and charac-
terize how changes with different species (Napoleon et al., 2013;
Uitz et al., 2010), depths, and seasons, and if value can be effectively
55
estimated from remotely sensible data. All these objectives demand
appropriate, and concurrent, measurements of PP and the optical
properties.
7.4. In situ measurement of primary productivity
Because it is the at-sea in situ PP that is used as a base for the scale
up for basin-scale estimates, it is critical to have accurate in situ mea-
surements of primary productivity. The topic of the measurement of
PP has been reviewed many times, and recently by Marra (2002,
2009), and the reader is referred to those publications for a more ex-
tended analysis. Here, we can categorize the measurement on the basis
of the scale of the measurement, and the kind of incubation container.
Traditionally, the incubation container has been a transparent bottle of
some kind or size that isolates a water sample from the environment so
that physiological measurements can be made, using isotopes of ele-
ments (13C, 14C, 18O), or the uxes of the molecules themselves (O2,
CO2), involved in photosynthesis. Recently, methods have been devel-
oped that allow the mixed layer itself to be the container, using iso-
topes of oxygen to estimate PP, and also net community production
(e.g., Quay et al., 2012). The advantage of the former method is that
the water sample is perfectly isolated, however, the containers are usu-
ally very small, and incubation time is short relative to how the ocean is
viewed by satellite. There may be deleterious effects from the enclosure
of a water sample for any length of time.
The advantage of the latter method is a broader scale, both in depth
(the mixed layer) and time (12 weeks) that may be more amenable to
scaling up to the scale of remote sensing. However, the larger container
is also more dynamic, and leaky. Mixed layer depth can easily change
diurnally, and day-by-day, limiting the environments for which the in
situ isotope methods can be employed. Too, exchanges across the base
of a mixed layer cannot be easily measured or estimated. Finally, the
depth of the euphotic zone usually extends beyond the mixed layer,
and those depths are typically characterized by a chlorophyll-a
maximum contributing to water column productivity.
A third alternative exists, uorescence kinetics, in the method of fast
repetition rate uorometry (FRRF), or pulse-amplitude modulated
(PAM) uorescence. These measurements are relatively simple, and
do not require incubation. Recent reports suggest that there is a mean-
ingful correlation between FRRF measurements and the photosynthetic
assimilation of 14C (Cheah et al., 2011), thus FRRF measurements could
serve as a simple mapping variable for larger-scale distributions of PP.
Moreover, since all PP algorithms currently use PP estimates from 14C
assimilation, there would be a means to extend the measurements in
space, at least to the extent of shipboard coverage.
Comparisons among these measurement options are rare or non-
existent. The mixed layer measurements are usually accomplished
without direct comparisons with incubation technologies, and vice-
versa. If we are to reach the goal of accurate assessments of PP for the
global ocean, a research program will be required that incorporates as
many different methods to estimate PP in a given environmental
setting. Perhaps something analogous to NOAA's MOBY program (see
http://moby.mlml.calstate.edu/) for validation of PP would be a good
start.
7.5. Improving the description of the vertical distribution of IOPs
Another important factor for accurate PP estimation is the vertical
distribution of the water properties (Platt et al., 1988; Sathyendranath
and Platt, 1989). The above discussion has assumed that the water col-
umn is well mixed. For natural waters, however, this assumption is not
always valid. For stratied waters, vertical variation in water properties
needs to be taken into account (Sathyendranath and Platt, 1989). In the
current models (Chl-based model) that include the vertical variation,
the attenuation coefcient is deduced from the vertical distribution of
phytoplankton biomass (Sathyendranath and Platt, 1993), with the
56 Z. Lee et al. / Journal of Marine Systems 149 (2015) 5059
vertical distribution of biomass collected from eld surveys (Morel and
Berthon, 1989; Platt et al., 1988). Recent eld measurements have
found that the vertical distribution of the optical properties do not nec-
essarily follow the same phase as that of phytoplankton biomass, mainly
because the vertical distribution of gelbstoff can be independent of bio-
mass (Siegel and Michaels, 1996). Since it is the optical properties that
determine the vertical propagation of solar radiation, information on
the vertical distribution of the optical properties is an important compo-
nent for improving PP estimation. Data banks that contain (or remote-
sensing methods to derive) the vertical distribution of aph, a, and bb
are strongly needed. If no such datasets exist for a given region, dynamic
models (e.g., Chai et al., 2002) are a useful alternative to generate appro-
priate vertical proles of these properties.
Acknowledgements
Financial support from NASA (NNX14AM15G) and NOAA (DG-133E-
13-SE-1669) are greatly appreciated. We are also extremely grateful for
the comments and suggestions from two anonymous reviewers.
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